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Lezama-García, K.;  Mota-Rojas, D.;  Martínez-Burnes, J.;  Villanueva-García, D.;  Domínguez-Oliva, A.;  Gómez-Prado, J.;  Mora-Medina, P.;  Casas-Alvarado, A.;  Olmos-Hernández, A.;  Soto, P.; et al. Thermoregulatory Mechanisms in Altricial and Precocial Species. Encyclopedia. Available online: https://encyclopedia.pub/entry/24766 (accessed on 05 September 2024).
Lezama-García K,  Mota-Rojas D,  Martínez-Burnes J,  Villanueva-García D,  Domínguez-Oliva A,  Gómez-Prado J, et al. Thermoregulatory Mechanisms in Altricial and Precocial Species. Encyclopedia. Available at: https://encyclopedia.pub/entry/24766. Accessed September 05, 2024.
Lezama-García, Karina, Daniel Mota-Rojas, Julio Martínez-Burnes, Dina Villanueva-García, Adriana Domínguez-Oliva, Jocelyn Gómez-Prado, Patricia Mora-Medina, Alejandro Casas-Alvarado, Adriana Olmos-Hernández, Paola Soto, et al. "Thermoregulatory Mechanisms in Altricial and Precocial Species" Encyclopedia, https://encyclopedia.pub/entry/24766 (accessed September 05, 2024).
Lezama-García, K.,  Mota-Rojas, D.,  Martínez-Burnes, J.,  Villanueva-García, D.,  Domínguez-Oliva, A.,  Gómez-Prado, J.,  Mora-Medina, P.,  Casas-Alvarado, A.,  Olmos-Hernández, A.,  Soto, P., & Muns, R. (2022, July 03). Thermoregulatory Mechanisms in Altricial and Precocial Species. In Encyclopedia. https://encyclopedia.pub/entry/24766
Lezama-García, Karina, et al. "Thermoregulatory Mechanisms in Altricial and Precocial Species." Encyclopedia. Web. 03 July, 2022.
Thermoregulatory Mechanisms in Altricial and Precocial Species
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This entry is adapted from the peer-reviewed paper 10.3390/vetsci9050246

Thermoregulation in newborn mammals is an essential species-specific mechanism of the nervous system that contributes to their survival during the first hours and days of their life. When exposed to cold weather, which is a risk factor associated with mortality in neonates, pathways such as the hypothalamic–pituitary–adrenal axis (HPA) are activated to achieve temperature control, increasing the circulating levels of catecholamine and cortisol. Consequently, alterations in blood circulation and mechanisms to produce or to retain heat (e.g., vasoconstriction, piloerection, shivering, brown adipocyte tissue activation, and huddling) begin to prevent hypothermia. Determined mainly by physiological maturity, mammals can be classified into altricial and precocial species. Although altricial and precocial newborns have several mechanisms to maintain a stable body temperature, a sudden drop in temperature experienced at birth reduces vigor and affects their feeding ability. Consequently, the acquisition of immunoglobulins and the ingestion of nutrients that fuel thermogenesis are compromised.

thermoregulation body temperature brown adipose tissue animal welfare neonate welfare fetal welfare puppy foal welfare buffalo newborn IRT Thermoregulation Infrared thermography

1. Brown Adipose Tissue Activation (BAT)

Among the three types of adipose cells found in mammals (brown, white, and beige), BAT represents the least abundant but the one with the greatest thermogenic capacity, especially at birth [21]. Nonetheless, its quantity depends on the fetal development during gestation, the species (altricial or precocial), and the deposited anatomical site [22].
Unlike WAT, BAT has more mitochondria, high cytochrome Cc content, a vast vascular network [23][24], and BAT activation is mediated by uncoupling protein 1 (UCP1) [8]. UCP1s respond to the secretion of norepinephrine (NE) released by the sympathetic nerves and its action on β3 adrenoreceptors, whose effect is reversible through vagal stimulation (parasympathetic) [11][25]. Among other actions, NE promotes the proliferation of preadipocytes, the differentiation of mature adipocytes, regulates the expression of genes that encode UCP1, and increases mitochondrial mass. Altogether, NE actions contribute to heat generation through ATP synthesis by UCP1 [26] and lipolysis [27]. In the case of altricial species such as laboratory rodents, the relative percentage of BAT and white adipocytes can vary, depending on environmental and nutritional conditions, sex, and age. However, its remarkable plasticity allows retroperitoneal WAT to transform to BAT when exposed to cold [28].
An example of this was reported in 27 newborn deer mice (Peromyscus maniculatus) kept at a temperatures of 5 °C. BAT utilization increased by 42% (measured in terms of oxygen consumption), suggesting it is the only mechanism responsible for maintaining thermal stability during the first days of life [29]. Likewise, prenatal exposure to temperatures of 15 ± 4.2 °C on a female Darwin´s leaf-eared mouse (Phyllotis darwini) was shown to improve the thermoregulatory capacity of neonates, achieving higher body temperatures (32.3 ± 2.41 °C) compared to animals acclimated to an ambient temperature of 30 °C, which can be attributed to higher amounts of BAT and the increased expression of UCP1 in adipocytes [30]. Nevertheless, the characteristics and the properties of BAT may differ between lines of the same species. In a comparative study between B6 and A/J mice, it was found that cold stress only induced BAT activation in A/J mice due to genetic variability in the expression of UCP1 and adipogenesis. B6 mice are an inbred strain used to study obesity, a trait associated with BAT [31], while A/J mice are another strain with susceptibility to obesity and, together with B6 mice, have shown regional differences after adrenergic stimulation of UCP1 [32]. In B6 mice, a resistance of BAT induction has been reported by adrenergic stimulation, contrary to the A/J strain. In A/J mice, the UCP1 expression in the retroperitoneal fat at 60 days of age was higher than in B6 mice, with an induced activity of 71%, more active than interscapular BAT. In contrast, in B6 mice, the presence of BAT was lower than that found in A/J mice at one month of birth [33].
Additionally, the mother’s diet and body condition have also been associated with the functionality and pre- and post-natal development of BAT. A study with female C57/BL mice of 10 to 12 weeks of age observed that obese mothers fed a high-fat diet presented a deficient activity of BAT as a thermoregulator, where the activation and the expression of UCP1 and other proteins responsible for lipolysis had a lower oxygen consumption. In contrast, a deficient BAT activation was not observed in mice from dams with balanced diets [34].
On the other hand, species that are born with a low birth weight in relation to the average birth weight of the species or breed, like canine puppies, are more exposed to hypothermia because they have less adipose tissue. Moreover, when there is competition with littermates for access to a nipple/teat or a deficiency in colostrum intake at birth, there is a higher risk of hypoglycemia, which has important repercussions on neonatal survival [35][36].

2. Thermoregulation in Precocial Animals

Precocial animals, such as ruminants usually present a greater development of thermoregulatory mechanisms at birth, allowing them to maintain a constant body temperature, even in cold environments [37]. In these species, non-shivering thermogenesis is the most used mechanism in neonates. For example, in lambs (O. aries), approximately half of the cold-induced summit metabolic rate comes from non-shivering thermogenesis. The presence of metabolic-active BAT during the early postnatal period is essential [38]. However, adipose tissue distributed in the pre-scapular, inguinal, and prerenal regions represents only 2% of the total body weight [25][39].
The thermogenic activity has been measured in perirenal adipose tissue from newborn lambs (O. aries) for up to 33 days. In these animals, the impact of cold acclimatization of the pregnant dams can influence the thermogenic capacity of the offspring. In lambs from mothers exposed to cold climates, they had a 21% greater perirenal fat, increased metabolic activity (40%), and higher oxygen consumption in cold temperatures (16%). Additionally, the thermogenesis responses of these lambs were due solely to non-shivering thermogenesis, in contrast to lambs from dams not climatized to the cold [40]. The activation of BAT tissue responds to an increase in blood levels of cortisol, NE, and epinephrine. These catecholamines bind to beta-3-adrenergic receptors located in BAT, activating the UCP1 in the inner mitochondrial membrane. UCP1 and thermogenin increase the H+ ion flux at the mitochondrial level without ATP production [41]. Similarly, during birth, the plasma levels of hormones such as triiodothyronine (T3) and thyroxine (T4), triggered by the release of thyroid-stimulating hormone (TSH), increase metabolic consumption of adipose tissue to produce non-shivering thermogenesis [42]. In lambs, Schermer et al. [43] studied the thermoregulatory capacity of newborn lambs with fetal thyroidectomy. According to Litten et al. [44] and Silva [45], the thyroid hormone pathway for heat production is more developed in precocial species. Thyroid hormones are critical for the generation and the maintenance of body basal temperature (BBT), and even slight changes in hormone levels can affect BBT [45]. It has been observed that minor changes in thyroxine (T4) concentrations significantly impact body temperature [45][46]. BAT contains multiple enzymes called deiodinases, essential for converting T4 to active triiodothyronine (T3). In other words, BAT can generate T3, which is crucial for producing ATP and heat [47]. When exposed to cold stimuli, the enzyme 5-deiodinase type II is activated, converting T4 to T3. However, if T3 is not produced, UCP1 synthesis is blocked, leading to hypothermia [48].
Due to the influence of thyroid hormones in thermoregulation [44][45], thyroidectomized animals presented lower colon temperatures (up to 2.35 °C) than control animals. For example, Berthon et al. [49] found that in pigs, lower plasma levels of T4 are present in animals with a lower rectal temperature after birth. Likewise, the thyroidectomized animals had a lower oxygen consumption rate and a higher incidence of shivering thermogenesis, which coincides with a lower activity of the perirenal adipose tissue, lower levels of uncoupling protein, and a higher lipid content.
In most mammals, concurrently with non-shivering thermogenesis, colostrum intake in the first hours of life represents an energy resource that contributes to maintaining a stable temperature in neonates [2]. In particular, the nutrients present in colostrum provide water, bioactive compounds, growth factors, digestive enzymes, and immunoglobulins, and one of its main roles during the first days after birth is the supplement of energy in the form of kcal/L. Although it is said that the nutritional properties of colostrum and milk are similar during the first days of life, the energy value of colostrum can be 20–30% higher than the values registered after three days or two weeks [50]. Additionally, colostrum intake and glucose absorption prevent hypoglycemia due to the low fat and glycogen storage in newborns [51], maintaining normal glucose levels that can support thermogenesis [52]. For example, in calves, colostrum provides large amounts of glucose and amino acids, equivalent to 6.7 MJ/g, that can be used to produce heat [42][53]. Piglets (S. scrofa) are a species born with low amounts of BAT; their main ways of heat production rely on shivering and colostrum intake shortly after birth [54]. Furthermore, several molecular (e.g., the presence of uncoupling proteins 1, 2, or 3, the responsible for non-shivering thermogenesis), ultrastructural (e.g., number of mitochondria in longissimus thoracis and rhomboideus muscle per unit tissue area), biochemical (e.g., fat oxidation, mitochondrial processes), physiological, and metabolic adaptations in the maturation of the energy production of the musculoskeletal system in piglets are an adaptive thermoregulatory mechanism [54]. Additionally, newborn piglets use their body fat and glycogen stores to survive in the first 12 to 24 h after birth [55].
On the other hand, the fetal development of BAT, the mother’s diet during gestation, and the influence of hormones such as melatonin have been shown to influence the thermoregulation capacity of the newborn. The case of 5 to 6-day-old lambs born from dams with low melatonin profiles and exposed to 4 °C showed a reduction in BAT temperature of approximately 39.8 °C compared to the control group of 40 °C and elevated NE concentrations greater than 1000 pg/ml, as a result of thermal stress [56].
Thermogenesis by BAT activation is essential in the neonate of most species, and it is also essential in hibernating animals such as American black bears (Ursus americanus) [57][58], which represents the first resource during the postnatal period. However, for species with limited energy reserves at birth, such as newborn piglets with low amounts of BAT or rodent pups with non-fully developed interscapular BAT, colostrum intake and other mechanisms to preserve heat are critical to prevent hypothermia.

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Subjects: Agriculture, Dairy & Animal Science
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Karina Lezama-García
,
Daniel Mota-Rojas
,
Julio Martínez-Burnes
,
Dina Villanueva-García
,
Adriana Domínguez-Oliva
,
Jocelyn Gómez-Prado
,
Patricia Mora-Medina
,
Alejandro Casas-Alvarado
,
Adriana Olmos-Hernández
,
Paola Soto
,
Ramon Muns
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Update Date: 07 Jul 2022
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